Intraembryonic hematopoietic cell migration during vertebrate development.

TLDR

In vertebrates, hematopoietic stem cells arise from ventral mesoderm and are thought to migrate to extra‑ and intra‑embryonic sites during gastrulation and neurulation, but intra‑embryonic migration has not been visualized, and in zebrafish hematopoiesis occurs solely in the dorsal intermediate cell mass rather than yolk‑sac islands. Using GATA‑1 and GATA‑2 markers, we showed that the zebrafish intermediate cell mass originates from posterior‑lateral mesoderm on the yolk syncytial layer and that its cells migrate anteriorly along the embryo before circulation, supporting a model in which vertebrate hematopoiesis is shaped by divergent migration routes of extra‑ and intra‑embryonic progenitors.

Abstract

Vertebrate hematopoietic stem cells are derived from vental mesoderm, which is postulated to migrate to both extra- and intraembryonic positions during gastrula and neurula stages. Extraembryonic migration has previously been documented, but the origin and migration of intraembryonic hematopoietic cells have not been visualized. The zebrafish and most other teleosts do not form yolk sac blood islands during early embryogenesis, but instead hematopoiesis occurs solely in a dorsal location known as the intermediate cell mass (IM) or Oellacher. In this report, we have isolated cDNAs encoding zebrafish homologs of the hematopoietic transcription factors GATA-1 and GATA-2 and have used these markers to determine that the IM is formed from mesodermal cells in a posterior-lateral position on the yolk syncytial layer of the gastrula yolk sac. Surprisingly, cells of the IM then migrate anteriorly through most of the body length prior to the onset of active circulation and exit onto the yolk sac. These findings support a hypothesis in which the hematopoietic program of vertebrates is established by variations in homologous migration pathways of extra- and intraembryonic progenitors.